Querleu 2017

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Ann Surg Oncol

DOI 10.1245/s10434-017-6031-z

ORIGINAL ARTICLE – GYNECOLOGIC ONCOLOGY

2017 Update on the Querleu–Morrow Classification of Radical


Hysterectomy
Denis Querleu, MD1, David Cibula, MD2, and Nadeem R. Abu-Rustum, MD3,4

1
Department of Surgery, Institut Bergonié, Bordeaux, France; 2Charles University, Prague, Czech Republic; 3Department
of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY; 4Weill Cornell Medical School, New York, NY

ABSTRACT Conclusion. Studies evaluating radicality in the surgical


Background. One of the most important principles in management of cervical cancer should be based on precise,
modern cervical cancer surgery is the concept of tailoring universally accepted descriptions. The authors’ updated
surgical radicality. In practice, this means abandoning the classification presents standardized, universally applicable
‘‘one-fits-all’’ concept in favor of tailored operations. The descriptions of different types of hysterectomies performed
term ‘‘radical hysterectomy’’ is used to describe many worldwide, categorized according to degree of radicality,
different procedures, each with a different degree of radi- independently of theoretical considerations.
cality. Anatomic structures are subjected to artificial
dissection artifacts, as well as different interpretations and
nomenclatures. This study aimed to refine and standardize One of the most important principles in modern cancer
the principles and descriptions of the different classes of surgery is the concept of tailoring surgical radicality. In
radical hysterectomy as defined in the Querleu–Morrow practice, this means abandoning the ‘‘one-fits-all’’ concept
classification and to propose its universal applicability. in favor of tailored operations. Wide surgical excision has
Methods. All three authors independently examined the been validated for a number of tumors including melano-
current literature and undertook a critical assessment of the mas and sarcomas as well as head and neck, breast, and
original classification. Images and pathologic slides vulvar cancers. In surgery for cervical cancer, adaptation
demonstrating different types of radical hysterectomy were of radicality according to preoperative estimation of tumor
examined to document a consensual vision of the anatomy. location, surgical margin, and risk of occult lymphatic
The Cibula 3-D concept also was included in this update. spread, which may be high for bulky tumors1 or negligible
Results. The Querleu–Morrow classification is based on in the setting of low-volume disease,2 has led to the
the lateral extent of resection. Four types of radical hys- development of ultra-radical cervical cancer surgeries on
terectomy are described, including a limited number of the one hand and more limited surgeries on the other.
subtypes when necessary. Two major objectives remain However, the term ‘‘radical’’ or ‘‘extended’’ hysterec-
constant: excision of central tumor with clear margins and tomy currently is used to describe a variety of different
removal of any potential sites of nodal metastasis. procedures, each entailing a different degree of radicality.
A variety of terms are currently applied to the same ana-
tomic structures. Anatomic structures currently are defined
according to different interpretations of the anatomy. Fur-
thermore, original descriptions change over time. Finally,
Electronic supplementary material The online version of this the addition of minor surgical variants—not all of them
article (doi:10.1245/s10434-017-6031-z) contains supplementary original—add to the confusion.
material, which is available to authorized users.
A classification of radical hysterectomies published in
20083 was adopted by the National Comprehensive Cancer
 Society of Surgical Oncology 2017
Network (NCCN) and appears in the NCCN clinical
First Received: 1 June 2017 practice guidelines.4 In 2011, a three-dimensional (3D)
anatomic template for radical lateral parametrectomy was
D. Querleu, MD proposed.5 We aimed to reconcile the two latter studies,
e-mail: [email protected]
D. Querleu et al.

further standardize the anatomic nomenclature, and refine pillar and the mesorectum, medial to the autonomic
the technical descriptions of the different procedures. nerves (Fig. S2), with the goal of preserving bladder
innervation. The medial pararectal space differs from
METHODS the Latzko pararectal space, which is developed
between the rectum medially, the sacrum dorsally,
Anatomic Nomenclature and the internal iliac vessels laterally.
3. The term ‘‘lateral parametrium’’ refers to the parac-
The international anatomic nomenclature can be found ervix. Therefore, we use both terms in this report.
in Terminologia Anatomica (TA)6,7 and should be used Notably, the structure empirically called paracolpos or
wherever it clearly applies. The widely used terms ‘‘ante- paracolpium is included in the paracervix in the TA
rior/posterior,’’ ‘‘deep/superficial,’’ and ‘‘internal/external’’ nomenclature because no border exists between lateral
are confusing. These should be replaced respectively by attachments of the cervix or the vagina. The paracervix
ventral/dorsal, caudal/cranial, and medial/lateral. is a complex structure with a heterogeneous anatomy
The dorsolateral attachment of the cervix is known as that has an impact on surgical management (Figs. 1,
the paracervix. This term should replace numerous other S3). The paracervix contains the main blood and
terms, including ‘‘cardinal ligament’’ or ‘‘Mackenrodt’s lymphatic vessels of the uterine cervix and comprises
ligament’’ (it is not a ligament). However, the term ‘‘me- two parts: the medial part, which is more condensed
sometrium,’’ including the anatomic parametrium and and fibrous, and the lateral part, which is composed of
paracervix, is an accurate correlation with the term ‘‘me- soft lymph node-bearing fatty tissue surrounding
sorectum’’ (used in rectal cancer surgery) because it refers vessels and nerves. The most stable anatomic land-
to the area at risk for discontinuous spread of cervical mark delineating the boundary between the two parts is
carcinoma. It has been associated with a functional view of the distal ureter (Fig. S1). The deep uterine vein
cancer spread based on embryologic development, a con- invariably runs cranial and perpendicular to the
cept that deserves consideration but remains hypothetical.8 hypogastric plexus (Fig. 2). However, the number of
Strict use of TA nomenclature is not necessarily appli- uterine veins may vary, and the deep uterine vein does
cable in surgical practice, in which different structures are not exactly represent the caudal limit of the paracervix.
created by surgical dissection and separated by artificially Figure 2 shows cellular paracervical tissue caudal to
created spaces. We describe these as follows: the deep uterine vein. The node-bearing tissue of the
lateral part of the paracervix can be removed with
1. The ‘‘ventral parametrium’’ is defined after surgical
preservation of the vessels and nerves as in any lymph
opening and development of two surgical spaces: the
node dissection. As stated by Palfalvi and Ungar,11
vesicouterine and vesicovaginal septum medially and
‘‘the border between parametrial dissection and lym-
the medial paravesical space laterally. The medial
phadenectomy is artificial and can be located in
paravesical space is developed medial to the lateral
ligament of the bladder, which contains the umbilical
and superior vesical arteries (Fig. S1). The medial
vesical space differs from the lateral (Latzko) par-
avesical space, which is developed between the
umbilical ligament and the external iliac vessels. The
ventral parametrium can be surgically divided into two
portions: one in the plane medial to the terminal ureter
(vesicouterine ligament cranial to the ureter and
vesicovaginal ligament caudal to the ureter) and the
other lateral to the plane of the ureter. The bladder
nerves run caudally and parallel to the ureter. Some
Japanese authors refer to the vesicovaginal ligament as
the ‘‘posterior leaf of the vesicouterine ligament.’’9
2. The ‘‘dorsal parametrium’’ is a complex structure
composed of the rectouterine and rectovaginal liga-
Deep uterine vein Inferior
ments (rectal pillar) and the dorsal part of the pelvic hypogastric plexus
autonomic nerves. A medial pararectal space (other-
wise described as the sacrouterine space or Okabayashi FIG. 1 Paracervix showing deep uterine vein and inferior hypogas-
space10) can be artificially created lateral to the rectal tric plexus. Courtesy of Dr. Ghislaine Escourrou, University Hospital,
Toulouse, France
Querleu–Morrow Classification: Hysterectomy

Deep uterine vein B1


C
Paracervix

B2
Inferior hypogastric
plexus
A

B
D
Ureter

FIG. 2 Cellular yellow paracervical tissue caudal to the deep uterine


FIG. 3 Lateral extent of resection. Courtesy of Pr. Brigitte Mauroy,
vein (left side of pelvis)
Institute of Anatomy, University of Lille, France. From Querleu and
Morrow3

different planes, but the same connective tissue is


extirpated.’’ Unless gross disease is present, the
question of how to excise the lateral part of the
paracervix can be solved by the concept of parametrial
node dissection.12,13

Updating Process

We aimed to refine the principles and description of the


different classes of radical hysterectomy defined in the
Querleu–Morrow classification. All three authors inde-
pendently examined the current literature and undertook a
critical assessment of the original classification. Imaging
and pathologic slides demonstrating different types of FIG. 4 Specimen of resected paracervix. Right Type B. Left Type A
radical hysterectomy were examined. The Cibula 3-D
concept,5 which has an impact on the definition of parac-
ervical excision in the type C procedure described later, has trials testing the safety of reduced radicality. It can be used
been included in this update. for (1) the management of selected low-risk IB1 invasive
cervical cancers smaller than 2 cm with negative pelvic
RESULTS nodes, no deep stromal invasion, and no lymph-vascular
space invasion and (2) the occasional completion surgery
Proposed Updated Classification for advanced cervical cancers after radiation,
chemotherapy, or both.
The Querleu–Morrow classification3 is based, for the Existing evidence indicates that pelvic node involve-
purpose of simplification, on the lateral extent of resection ment is a major independent predictor of parametrial
only (Fig. 3). Stable anatomic landmarks, such as the involvement. This factor is not always identified at the time
crossing of the ureter with the uterine artery and parac- of surgery. However, in some centers, routine frozen sec-
ervix, and the vascular plane of the internal iliac system are tion of sentinel nodes (or side-specific lymph node
used to define the limits of resection. dissection when no sentinel nodes are detected on a given
pelvic sidewall) is used as a decision tool, with excellent
Type A: Limited Radical Hysterectomy This tailored results.14 In other centers, tailoring is less practical. A less
procedure (Fig. 4) is not accessible to general than radical surgery may be problematic if it is not known,
gynecologists without training in radical surgery. The with reasonable confidence, that the pelvic nodal status is
goal of the operation is to ensure removal of the cervix in negative.
its entirety down to the vaginal fornix, together with a Type A is not a simple ‘‘extrafascial’’ hysterectomy. The
paracervical margin. This is crucial to the design of future position of the ureters must be determined by direct
D. Querleu et al.

visualization (after opening of the ureteral tunnels) at the resection. Approximately 10 mm of the vagina from the
time of abdominal or laparoscopic surgery or by palpation caudal edge of the cervix or tumor is resected, without
at the time of vaginal surgery. The uterine pedicles can be intent to radically resect the paravaginal tissues. The
transected at their crossing with the ureter, as in the orig- vesicovaginal ligament is not resected. As a result, the
inal Wertheim operation, or at their origin. The paracervix bladder nerves, which run within the vesicovaginal liga-
is transected medial to the ureter but lateral to the cervix. ment caudal to the ureter and lateral to the vaginal fornix,
The paracervix is excised halfway between the ureter and are not at risk. The radicality of this operation can be
the cervix and caudally parallel to the cervix until the increased without increasing the risk of hypogastric nerve
lateral vaginal fornix is reached and opened. Kinking or injury.
thermal injury of the distal ureter (related to the en bloc use Although the type B1 procedure does not involve
of heat-generating devices) is a concern because the ureter resecting the nodes of the lateral part of the paracervix, a
is not fully mobilized. The rectovaginal ligaments and the paracervical lymphadenectomy can be added to increase the
vesicouterine ligaments are defined, then divided at a dis- radicality of node dissection. This results in a type B2
tance from the uterus, but not at the rectum or bladder. This resection. Combined with pelvic lymphadenectomy, type
involves an approximate 5-mm resection of the corre- B2 surgeries aim to remove the pelvic nodes as completely
sponding ligaments. No removal of the vaginal part of the as possible. In this context, resection of the nodes located
paracervix (paracolpos) is involved. Vaginal resection is caudal to the obturator nerve and cranial to the sciatic nerve
minimal, routinely less than 10 mm. is part of the additional paracervical lymphadenectomy.
Obtaining a free exocervical margin without any inva- Adding a lateral paracervical nodal dissection to a
sive or preinvasive disease is a major objective of surgery proximal-type radical hysterectomy improves lateral radi-
in the setting of early cervical cancer. Although colpec- cality without increasing morbidity.8,12,13 The gluteal and
tomy may constitute overtreatment in some cases, without pudendal nodes, which are caudal and lateral to the iliac
it there is a risk of involved margins or even incomplete vessels, are included in the template. The procedure may be
resection of the cervical stroma. However, patients with refined by the use of indocyanine green navigation, which
preoperative in sano cone biopsy could be spared allows the surgeon to identify the lymph vessel and lymph
colpectomy. node component of the paracervix more clearly.15
Our goal is to define a new surgical option (i.e., ‘‘min- The goal is to incorporate recent developments associ-
imal radical surgery’’), which is a smaller operation than ated with the use of ICG navigation, as published by others.
the standard modified radical hysterectomy (type B, We do not take sides in this regard because our objective is
described in the next section), but a larger operation than a to make the proposed classification system adaptable to
simple or extrafascial hysterectomy/trachelectomy. In recent surgical variations.
general, we do not recommend any specific type of surgical
radicality for every clinical situation. Although the trend Type C: Transection of the Paracervix at Its Junction
toward conservative surgery in the setting of early cervical with the Internal Iliac Vascular System This operation
cancer may be justified, to date, no definitive evidence corresponds to the classical radical hysterectomy. It is
ensures that ‘‘simple’’ procedures are safe. Furthermore, we adapted to International Federation of Gynecology and
are concerned about disseminating the idea that early cer- Obstetrics (FIGO) stage IB1 lesions with deep stromal
vical cancer can be managed using a common, non-radical invasion and IB2-2A or early 2B cervical cancers. The
procedure. We fear that this may lead to suboptimal lateral border is defined as the medial aspect of the internal
surgeries without adequate preoperative staging in non- iliac artery and vein.
specialized settings. Transection of the rectovaginal and rectouterine liga-
ments is performed at the rectum. Transection of the
Type B: Resection of the Paracervix at the Ureter This ventral parametrium ligament is performed at the bladder.
operation (Figs. 4, S4) includes two subtypes: types B1 and Both the vesicouterine and vesicovaginal ligaments are
B2. Type B1 is the ‘‘modified’’ radical hysterectomy. The resected. The ureter is completely mobilized and lateral-
ureter is unroofed and mobilized laterally, permitting ized. The length of the vaginal cuff is adjusted to the
transection of the paracervix at the level of the ureteral vaginal extent of the tumor.
tunnel. In type C procedures, the decision about autonomic
The caudal limit must not involve the inferior nerve preservation is crucial. Two subcategories are
hypogastric plexus (Fig. S4). Partial resection of the uter- defined in the following sections.
osacral peritoneal fold of the rectouterine ligament (dorsal
parametrium) and the vesicouterine (ventral parametrium) Type C1: Nerve-preserving Radical Hysterectomy The
ligament also is a standard component of this dorsal parametrium is transected after the dorsal segment
Querleu–Morrow Classification: Hysterectomy

of the autonomic nerve system has been separated Höckel.16 It usually is performed for laterally recurrent
(Fig. S2). The inferior hypogastric plexus is systematically tumors as a separate procedure.
identified and preserved by transecting only the uterine Table 1 defines the different classes of radical
branches of the pelvic plexus at the time the lateral para- hysterectomy.
metrium is transected. Ventrally, the bladder branches of
the pelvic plexus are preserved in the vesicovaginal liga- DISCUSSION
ment. Then, only the medial part of the ventral
parametrium is resected, and the bladder branches of the The popular Piver–Rutledge–Smith classification,17
hypogastric plexus caudal to the course of the ureter are published in 1974, describes five classes of radical hys-
identified and preserved. terectomy. The original paper does not refer to clear
anatomic landmarks and international anatomic definitions.
Type C2: No Preservation of Autonomic Nerves The Excessive vaginal resections, from one third to three
paracervix is completely transected. The inferior fourths of the vagina, are included in some templates. Class
hypogastric plexus, together with the sacral splanchnic 1 is not a radical hysterectomy, and class 5 is no longer
nerves, is divided lateral to the rectum. Type C2 requires a used. The rationale and anatomy differentiating classes 3
complete dissection of the ureter from the ventral and 4 are not clear. Finally, the Piver–Rutledge–Smith
parametria (vesicovaginal ligament). The ventral parame- classification applies only to open surgery and was devel-
tria are resected at the level of the bladder wall (Fig. S5). oped at a time when minimally invasive and fertility-
Bladder branches of the hypogastric plexus are sacrificed, sparing operations did not exist. It fails to take into account
so it is not necessary to identify them. Laterally, the the concept of nerve preservation and ignores the vaginal
resection continues alongside the medial aspect of the approach.
internal iliac vessels down to the pelvic floor. An interesting tumor-node-metastasis (TNM)-like
The medial pararectal (sacrouterine), lateral pararectal, description of the operation that defines three classes of
and lateral paravesical spaces are unified by transecting the radicality in all directions has been developed.18 However,
pelvic attachment of the paracervix together with the the model results in 91 possible subtypes.
splanchnic nerves in the caudal part (Fig. S6). Parts of the Two metrics define the outcomes of radical hysterec-
vaginal component of the paracervix (paracolpium) are tomy: (1) adverse effects such as bladder and rectal
removed. The removal of the dorsal parametrium is dysfunction and (2) the curative effect of the surgery.
extended caudally to the sacral attachment. The more extensive the surgery is, the higher the risk of
Type C is the standard operation for bulky or high-risk complications. However, small surgeries may undertreat
tumors. Type C1 has become the mainstay. Type C2 can be high-risk tumors, whereas big surgeries may overtreat
justified only for anatomic reasons. low-risk tumors. The Querleu–Morrow classification
provides a simple and universal tool for assigning dif-
Type D: Laterally Extended Resection These less ferent levels of radicality to a limited number of
common surgeries feature additional ultra-radical categories. Some surgeries may be asymmetric. The
procedures, in which structures lateral to the paracervix same classification applies to fertility-sparing surgeries
are resected. Two subtypes are described in the following (type B, as in the Dargent operation, and type A in new
sections. variants adapted to minimal disease or after neoadjuvant
Type D1: Resection of the Entire Paracervix at the chemotherapy).
Pelvic Sidewall Together With the Hypogastric and Because it is impossible to describe all variations of
Obturator Vessels, Exposing the Roots of the Sciatic these procedures, the use of a simple classification system
Nerve. The resection plane is lateral to the internal iliac does not preclude a careful description of any single
vessels, interrupting branches of gluteal superior, gluteal operation. The list of required information should be a
inferior, and pudendal vessels. This procedure corresponds component of quality control in the surgical management
to the Palfalvi–Ungar laterally extended parametrectomy11 of cervical cancers. The following items should appear in
and may be used for stage 2B tumors. the operative report:
Type D2: D1 Plus Resection of the Adjacent Fascial/
• All components defining the type of radical hysterec-
Muscular Structures. These structures include, when nec-
tomy. The management of the lateral, ventral, and
essary, the obturator fascia and obturator muscle ventrally,
dorsal attachments of the cervix must be described.
the coccygeus muscle and pelvic part of the piriformis
• Mode of management of the uterine artery, which is
muscle dorsally, and the sacrospinous ligament and
routinely divided at its origin from the internal iliac
acetabulum laterally. This procedure corresponds to the
artery but may be divided at the ureter in type A
laterally extended endopelvic resection described by
D. Querleu et al.

TABLE 1 Summary of the main landmarks in each type of radical hysterectomy on each part of the parametria
Dimension Paracervix or lateral parametrium Ventral parametrium Dorsal parametrium
Type of
radical
hysterectomy

A Halfway between the cervix and ureter Minimal excision Minimal excision
(medial to the ureter–ureter identified
but not mobilized)
B1 At the ureter (at the level of the ureteral Partial excision of the vesicouterine ligament Partial resection of the
bed–ureter mobilized from the cervix rectouterine-rectovaginal
and lateral parametrium) ligament and uterosacral
peritoneal fold
B2 Identical to B1 plus paracervical Partial excision of the vesicouterine ligament Partial resection of the
lymphadenectomy without resection rectouterine-rectovaginal
of vascular/nerve structures ligament and uterosacral fold
C1 At the iliac vessels transversally, caudal Excision of the vesicouterine ligament at the At the rectum (hypogastric nerve
part is preserved bladder. Proximal part of the vesicovaginal is dissected and spared)
ligament (bladder nerves are dissected and
spared)
C2 At the level of the medial aspect of iliac At the bladder (bladder nerves are sacrificed) At the sacrum (hypogastric nerve
vessels completely (including the is sacrificed)
caudal part)
D At the pelvic wall, including resection At the bladder. Not applicable if part of exenteration At the sacrum. Not applicable if
of the internal iliac vessels and/or part of exenteration
components of the pelvic sidewall

(management of the adjacent lymph node-bearing CONCLUSION


tissue).
• Assessment of the surgical and pathologic length of the Radical hysterectomy is not a single operation. The
lateral extent of the resection. The surgical length variations of this procedure must balance curative effects
should be measured on the fresh specimen without with the risk of adverse consequences. An internationally
stretching. The pathologic length should be measured accepted classification system of radical hysterectomy that
after fixation. However, the ventral and dorsal dimen- will be accepted and used by individual surgeons, study
sions are difficult to assess. Measurements should be groups, and national and international societies is clearly
taken independently by someone other than the needed. Evaluation of techniques and quality control
surgeon. should be a basic component of every surgical activity.
• The surgical and pathologic minimum length of vagina To date, no evidence exists to support any recommen-
removed and, when applicable, the minimum distance dation regarding the distance from central tumor to
between the tumor and the margin of resection. Again, margins. Only one randomized, controlled study has
measurements should be taken independently on the compared less extensive primary surgeries with more
fresh specimen, without stretching, after fixation. extensive primary surgeries in terms of morbidity, overall
• In fertility-preserving surgery, information regarding and disease-free survival, and relapse.20 However, the
the pathologic distance between the tumor and the study was underpowered to detect differences in outcomes
endocervical resection margin. for different stages and substages of early cervical cancer.
The manner in which hemostasis is achieved also must be In addition, a substantial proportion of the patients had
described to evaluate the impact of new techniques or undergone adjuvant radiation therapy, thus contradicting
devices on radicality and outcome, such as blood loss or the generally accepted principle that patients should be
complication rates. Notably, it has been demonstrated that spared the discomfort and potential complications associ-
the achievement of lateral resection is dependent on ated with combined surgery and radiation therapy.
hemostasis technique. This highlights the importance of The most precise indicator of the risk of occult lym-
technical improvements, irrespective of classification.19 A phatic involvement of pericervical structures, including the
precise description of technique should appear in the paracervix and the ventral and dorsal parametria, is
operative report. described in two studies of giant pathologic sections.21,22
Querleu–Morrow Classification: Hysterectomy

These studies suggest that the risk of visceral lymph node descriptions and nomenclature of the fasciae and ligaments of the
involvement is associated with tumor size and stage, female pelvis: a dissection-based comparative study. Am J Obstet
Gynecol. 2005;193:1565–73.
clearly supporting the concept that the extent of excision 8. Höckel M, Horn LC, Fritsch H. Association between the mes-
should increase, or widen, as stage and tumor size increase. enchymal compartment of uterovaginal organogenesis and local
However, both studies were based on specimens derived tumor spread in stage IB-IIB cervical carcinoma: a prospective
from type C operations. Neither study was designed to study. Lancet Oncol. 2005;6:751–6.
9. Fujii S, Tanakura K, Matsumura N, Higuchi T, Yura S, Mandai
document the clinical use of less radical surgeries for low- M, Baba T. Precise anatomy of the vesico-uterine ligament for
risk cervical cancers. radical hysterectomy. Gynecol Oncol. 2007;104:186–91.
Our proposed classification is not a guideline, but rather 10. Yabuki Y, Asamoto A, Hoshiba T, Nishimoto H, Satou N. A new
a standardized description of different surgeries performed proposal for radical hysterectomy. Gynecol Oncol.
1996;62:370–8.
worldwide, independent of underlying theoretical objec- 11. Palfalvi L, Ungar L. Laterally extended parametrectomy (LEP),
tives or the surgeon’s choice of approach in individual the technique for radical pelvic sidewall dissection: feasibility,
cases. Two major objectives are constant: (1) excision of technique, and results. Int J Gynecol Cancer. 2003;13:914–7.
the central tumor with clear margins and (2) removal of any 12. Höckel M, Konerding MA, Heussel CP. Liposuction-assisted
nerve-sparing extended radical hysterectomy: oncologic ratio-
potential site of node metastasis. Future randomized studies nale, surgical anatomy, and feasibility study. Am J Obstet
designed to document the need for extended or reduced Gynecol. 1998;178:971–6.
radicality in the surgical management of cervical cancer 13. Querleu D, Narducci F, Poulard V, Lacaze S, Occelli B, Leblanc
should be based on precise, universally accepted E, Cosson M. Modified radical vaginal hysterectomy with or
without laparoscopic nerve-sparing dissection: a comparative
descriptions. study. Gynecol Oncol. 2002;85:154–8.
14. Kyo S, Mizumoto Y, Takakura M, et al. Nerve-sparing abdominal
ACKNOWLEDGEMENT This study was funded in part through radical trachelectomy: a novel concept to preserve uterine bran-
the NIH/NCI Support Grant P30 CA008748 (Nadeem R. Abu- ches of pelvic nerves. Eur J Obstet Gynecol Reprod Biol.
Rustum). 2015;193:5–9.
15. Kimmig R, Aktas B, Buderath P, Rusch P, Heubner M. Intra-
DISCLOSURE Denis Querleu received travel expenses for the operative navigation in robotically assisted compartmental
2014 IGCS meeting (Melbourne) from Karl Storz GmBH. He has surgery of uterine cancer by visualisation of embryologically
consulted for Roche Inc. Other authors declares no conflicts of derived lymphatic networks with indocyanine-green (ICG). J
interest. Surg Oncol. 2016;113:554–9.
16. Höckel M. Laterally extended endopelvic resection: surgical
treatment of infrailiac pelvic wall recurrences of gynecologic
malignancies. Am J Obstet Gynecol. 1999;180:306–12.
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